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The effect of forest fuel harvesting on the fungal diversityof clear-cuts

Tero Toivanen a,*, Anni Markkanen b, Janne S. Kotiaho a,c, Panu Halme a

aCentre of Excellence in Evolutionary Research, Department of Biological and Environmental Science, PO Box 35,

FIN-40014 University of Jyvaskyla, FinlandbEcology and Evolutionary Biology, Department of Biological and Environmental Science, PO Box 35,

FIN-40014 University of Jyvaskyla, FinlandcNatural History Museum, P.O. Box 35, 40014 University of Jyvaskyla, Finland

a r t i c l e i n f o

Article history:

Received 17 February 2011

Received in revised form

23 November 2011

Accepted 24 November 2011

Available online 8 February 2012

Keywords:

Agarics

Boreal forest

Dead wood

Logging residues

Polypores

Stump removal

* Corresponding author. Tel.: þ358 14 260229E-mail address: tero.j.toivanen@jyu.fi (T.

0961-9534/$ e see front matter ª 2011 Elsevdoi:10.1016/j.biombioe.2011.11.016

a b s t r a c t

The removal of logging residues and stumps from clear-cuts has become a common

forestry practice. Forest fuel harvesting decreases the initially low volume of dead wood in

managed forests, but the biodiversity effects are poorly known. We studied the effects of

forest fuel harvesting on decomposer fungi on clear-cut Norway spruce stands in central

Finland. The number of occurrences and taxa of polypores, saprotrophic agarics and

pleurotoid agarics were determined on 10 forest fuel harvested and 10 control clear-cuts

4e5 years after logging. In total, we recorded 148 fungal taxa. The total number of taxa,

the number of polypore occurrences, and the number of polypore species within small area

were lower at forest fuel harvested sites. The effect on the number of saprotrophic agaric

taxa became obvious with increasing area. Most of the common polypore species had

fewer occurrences on forest fuel harvested sites while the commonest agaric species

increased due to forest fuel harvesting. Concerning different dead wood types, there were

fewer fungal species and occurrences on stumps and fewer occurrences on logs on forest

fuel harvested sites. Most of the effects of forest fuel harvesting were explained by the

reduction in resource availability. We conclude that forest fuel harvesting, especially

stump removal, has negative effects on decomposer fungi and that there is a risk that

populations of certain species still thriving in managed forests will decline in the future.

ª 2011 Elsevier Ltd. All rights reserved.

1. Introduction simplified the age and community structure of forest stands

Human activities have decreased the amount and diversity of

natural habitats and resources worldwide. Boreal forests in

Fennoscandia have been under forest management of

increasing intensity for centuries and today the majority of

forested area is managed for timber production. Human

impact has led to the loss and fragmentation of old-growth

forests, eliminated the effects of natural disturbances,

2; fax: þ358 14 2602321.Toivanen).ier Ltd. All rights reserve

and decreased the amount and quality of dead wood [1e3].

Because of these changes in forest dynamics and structure,

countless species, in particular those which depend on dead

wood, have become rare or threatened [4,5].

The interest to use wood-based energy has increased

because of the requirements of current climate and energy

policies [6]. Consequently, the extraction of logging residues

(treetops, branches) and stumps has become a common

d.

b i om a s s a n d b i o e n e r g y 3 9 ( 2 0 1 2 ) 8 4e9 3 85

practice in the forests of northern Europe but also in North

America [7,8]. In Finland, the greatest potential has been seen

in forest chips, which have so far been produced mainly from

logging residues from clear-cuts, but the use of stumps and

roots has increased rapidly and also small-diameter wood

from forest thinnings is used [9]. The aim of Finland’s National

Forest Program [6] is to triple the use of forest chips by 2015.

Harvesting of logging residues and stumps poses a potential

threat to biodiversity because it reduces the volume of dead

wood in managed forests and increases the intensity of the

disturbance. The magnitude of the change in dead wood

availability is high: forest fuel harvesting extracted 65% of the

logging residues in Swedish clear-cuts [10] and 42% of

branches and 81% of cut stumps in Finnish clear-cuts [11].

Dead wood is a key factor for diversity in boreal forests, as

it provides a habitat or a source of nutrients for a large number

of species [12e14]. One of themost species-rich groups among

dead wood dependent species is fungi [2]. As major decom-

posers of organicmatter, fungi play an important role in forest

ecosystem facilitating the nutrient cycle and acting as

ecosystem engineers that modify resources suitable for other

species [13,15]. Wood-inhabiting fungi contain a high number

of red-listed species (IUCN classes RE, CR, EN, VU and NT) and

they are commonly used as indicators for conservation value

of forests [13].

In managed boreal forests, there is 90e98% less coarse

woody debris (CWD, diameter �10 cm) than in natural forests

[2,16]. In contrast, the amount of fine woody debris (FWD,

diameter<10 cm) can be higher in managed forests [2,17]. The

majority of studies have focused on the volume and impor-

tance of CWD [18e20], and e.g. many red-listed fungi have

been shown to prefer large logs in intermediate decay stages

[21]. However, when equal volumes of FWD and CWD are

compared the species richness may be even greater on FWD

[22e24]. FWD is inhabited by a distinctive fungal community

[22,25] and its importance for species richness is emphasized

when the total amount of dead wood is low [23].

Early successional stages of boreal forests are known to

host particularly high species diversity, and several species

are specialized to these stages because of the warm, sun-

exposed conditions and the wealth of dead wood [26e28].

Today, early successional stages of natural origin are very rare

in Fennoscandia but they have been replaced by clear-cuts.

Although clear-cuts can by no means substitute the early

successional stages formed by natural disturbances, they

have been shown to be surprisingly species-rich habitats

where also red-listed species may occur [28,29]. This may be,

in addition to the physical conditions, due to there still being

remarkable quantities of dead wood which largely consists of

cut stumps and small-diameter logging residues [11]. Espe-

cially stumps harbour rich fungal flora, but the small-

diameter wood is important for hosting species which are

not found on the other substrates [28,30,31]. However, only

few red-listed fungi have been observed on logging residues or

stumps [18,20].

Forest fuel harvesting is likely to alter the fungal assem-

blages of clear-cuts. However, the actual effects are poorly

known, although there is some evidence that removal of

logging residues may decrease fungal diversity [32,33]. To fill

the knowledge gap, we established a comparative study to

determine how forest fuel harvesting affects decomposer

fungi. We studied the effects on three fungal groups: poly-

pores, saprotrophic agarics and pleurotoid agarics. We

compared clear-cuts where logging residues and stumps had

been harvested to standard clear-cuts where forest fuel har-

vesting had not taken place.

2. Material and methods

2.1. Study sites and experimental design

The study sites were located in central Finland near the city of

Jyvaskyla (Table 1). The sites were located within southern

boreal vegetation zone, except the northernmost site within

middle boreal zone [34]. The forests were owned by forest

company UPM, Metsahallitus, and city of Jyvaskyla.

We selected 20 sites that had been clear-cut in 2001 or 2002.

10 of the sites were clear-cuts where logging residues and

stumps had been harvested (forest fuel harvested; referred to

as FFH clear-cuts) and 10 were standard clear-cuts where

logging residues and stumps had been left (referred to as

control clear-cuts). All of the sites were ofmesicMyrtillus type

[35] and had been dominated by Norway spruce (Picea abies (L.)

Karst.). After clear-cutting, the sites had been planted for

spruce, birch (Betula spp.) or in one case for larch (Larix sibirica

Ledeb.). The size of the clear-cuts varied from 0.5 to 5 ha.

On each clear-cut, we established randomly four

20 m � 20 m square sample plots (in total 0.16 ha). First we

located a “centre point”, from which four 30 or 50 m lines

(length depending on the size of the clear-cut) were drawn to

randomly selected directions. The end point of each line

became the north-east corner of a sample plot. At some clear-

cuts of irregular shape we had to use two centre points or to

select the center point from the edge of the clear-cut to be able

to establish all four sample plots. The sample plots were not

established on locations that distinctly differed from the

surrounding clear-cut, such as on tracks or on rocks. The

sample plots also did not overlap or touch each other.

2.2. Sampling and classification of fungi

Wecarried out the fungi inventories in September 2006. Due to

the weather of summer 2006 being relatively dry, the number

of fungal occurrences was low in early September but

increased towards theendof themonth (Fig. 1). Sampleplots of

FFH and control clear-cuts were investigated by turns to keep

the effect of inventory date equal between treatments. Within

the sample plot, we inventoried the ground and all pieces of

dead wood with large-end diameter �2 cm and the large-end

located inside the sample plot. Fungi growing on stumps

standing on the edge of the sample plot were included.

For study species we selected fungal groups that are

ecologically important decomposers and that can be invento-

ried and identified with a reasonable effort. We excluded for

example sac fungi (Ascomycota) to reduce the work load. The

systematically surveyed taxa were polypores (non-gilled

bracket fungi; Polyporaceae sensu lato according to classifica-

tion of Niemela [36]) and decomposer agarics (gilled mush-

rooms that decompose organicmatter; Agaricales according to

Table 1 e The locations of the study sites.

Site Municipality Coordinates Treatment

Sammalsuo Orivesi 61� 470 5400’N 24� 440 5300’E Control

Pahajarvi NW Orivesi 61� 470 5600’N 24� 430 4200’E FFH

Haapala N (1) Jamsa 61� 470 5800’N 24� 460 5300’E Control

Ahvenjarvi W Orivesi 61� 470 5900’N 24� 440 5200’E FFH

Haapala N (2) Jamsa 61� 480 0300’N 24� 460 4700’E FFH

Haapala N (3) Jamsa 61� 480 0500’N 24� 460 4100’E Control

Pahajarvi N Orivesi 61� 480 0600’N 24� 440 0400’E FFH

Iso Kaukajarvi S (1) Orivesi 61� 480 1600’N 24� 440 0000’E FFH

Iso Kaukajarvi S (2) Orivesi 61� 480 1700’N 24� 430 5300’E Control

Kartiskajarvi S Orivesi 61� 480 1700’N 24� 450 0500’E Control

Iso Kaukajarvi S (3) Orivesi 61� 480 2500’N 24� 430 5100’E FFH

Toljussuo Jamsa 61� 480 4300’N 24� 470 2700’E FFH

Hiisimaki Jyvaskyla 62� 110 3200’N 25� 260 1400’E Control

Hiisimaki W Jyvaskyla 62� 110 3400’N 25� 260 0000’E Control

Naulamaki Jyvaskyla 62� 120 2600’N 25� 220 1400’E Control

Soidenlampi W Jyvaskyla 62� 130 0400’N 25� 380 0100’E FFH

Torvela Jyvaskyla 62� 140 1100’N 25� 240 3800’E Control

Tuohimaki NE (1) Petajavesi 62� 190 0600’N 25� 270 5500’E Control

Tuohimaki NE (2) Petajavesi 62� 190 1200’N 25� 270 6000’E FFH

Nurkkala Uurainen 62� 250 5200’N 25� 240 3200’E FFH

FFH ¼ forest fuel harvested clear-cut, control ¼ control clear-cut.

b i om a s s an d b i o e n e r g y 3 9 ( 2 0 1 2 ) 8 4e9 386

the classification of Kytovuori et al. [37]). Among decomposer

agarics, pleurotoid agarics (according to the classification of

Jakobsson and Niemela [38]) were treated as separate group

because they are ecologically distinct from other agarics and

typicallygrowondeadwood, and theotherspecieswerepooled

to form another group (referred to as saprotrophic agarics).

The number of occurrences was counted differently for

species growing on dead wood and species growing on forest

floor. Considering the species consistently growing on dead

wood (polypores and pleurotoid agarics), the fruit bodies of

a given species on one piece of dead wood are generally

regarded as one occurrence [20,28] and we used the same

approach. Considering the species growing also on forest floor

(saprotrophic agarics) it is difficult to define the area where

fruit bodies of the given species belong to the same individual.

Therefore, we regarded each fruit body as one occurrence.

As a rule, we identified polypores to species level. The

majority of agarics were also identified to species level.

However, some agarics (e.g. Entoloma spp.) were identified only

to genus level. Each of these genera was counted as one taxon.

Among some genera (e.g. Mycena spp.), some species of the

genus were identified to species level while other species

could only be identified to genus level. Among these genera,

each identified species was counted as one taxon, and those

identified to genus level were pooled to form one taxon.

We identified the fungi in situ or collected specimens for

microscopic identification (ca 1100 specimens). The voucher

specimens are preserved in the Natural History Museum of

University of Jyvaskyla (JYV). The nomenclature of polypores

follows Kotiranta et al. [39] and that of agarics follows Kyto-

vuori et al. [37].

Fig. 1 e The relationship between inventory date (1e31 [ 1

Septe1 Oct) and number of fungal taxa recorded on a study

plot on forest fuel harvested (black circles) and control

clear-cuts (open circles).

2.3. Dead wood data

Each occurrence of fungi on dead wood was recorded with

a classification of the dead wood substrate, the classes being

branches, logs (treetops and pieces of logs included), stumps,

pieces of stumps, roots and standing dead trees. In addition,

we carried out an extensive dead wood inventory on four

10 m � 10 m plots per site located within the fungi sample

plots. All pieces of dead wood with large-end diameter �2 cm

and length �20 cm were measured. We also recorded the tree

species, class (as described above), and decay stage of the dead

wood pieces and determined whether the pieces originated

b i om a s s a n d b i o e n e r g y 3 9 ( 2 0 1 2 ) 8 4e9 3 87

from the clear-cutting or from the pre-cutting period. The

dead wood inventory was carried out in May and June 2006

and the data has been published in [11].

2.4. Statistical analyses

2.4.1. Number of occurrences and taxa on FFH and controlclear-cutsThe response variables in the analyseswere 1) total number of

fungal taxa; 2) total number of polypore occurrences and

species, and number of occurrences of four commonest pol-

ypore species (Fomitopsis pinicola, Gloeophyllum sepiarium, Skel-

etocutis amorpha and Trichaptum abietinum); 3) total number of

saprotrophic agaric occurrences and taxa, and number of

occurrences of the commonest saprotrophic agaric species

(Hygrophoropsis aurantiaca); and 4) total number of pleurotoid

agaric occurrences and species. The number of species/taxa

was determined at two spatial scales: at the plot scale (0.04 ha)

and at the site scale (four sample plots; 0.16 ha).

The effects of forest fuel harvesting on the number of

species/taxa and occurrences at site scale were analyzed with

ANOVAwith inventory date as a covariate. The effect of forest

fuel harvesting on the number of species/taxa at plot scale

was analyzed with nested ANOVA into which treatment (FFH/

control) was entered as a fixed factor, study site nested within

the treatment as a random factor, and inventory date as

a covariate. Nested ANOVA was used because study plots

within one site are not independent replicates. Equal degrees

of freedommake the results directly comparable between the

scales.

We also compared the speciesearea relationships of FFH

and control clear-cuts by calculating sample-based species

accumulation curves with 95% confidence intervals. Study

plots were used as sub-samples. Separate curves were calcu-

lated for total number of taxa, number of polypore species and

number of saprotrophic agaric taxa. The curves were plotted

against area increasing up to 1.6 ha (10 sites).

Finally, we used multiple stepwise regression (enter crite-

rion p < 0.05, removal criterion p > 0.10) to explore whether

the number of fungal occurrences and species/taxa on a study

site could be predicted by dead wood variables. We formed

ecologically meaningful variables which were the volumes of

large logs (CWD, diameter�10 cm), small logs (FWD, diameter

<10 cm), stumps, branches, and old dead wood (originated

from the pre-cutting period, all classes included). In addition,

inventory date was included in the analysis.

2.4.2. Number of occurrences and taxa on different deadwood substratesWe determined the effect of forest fuel harvesting on the total

number of fungal occurrences and taxa recorded on three

commonest dead wood classes: logs, stumps and branches.

The treatment effect was analyzed with ANOVA with inven-

tory date as a covariate. Here we also tested whether there

was a treatment effect not related to resource availability. For

number of occurrences, this was done by entering the volume

of the dead wood substrate to the ANOVA as a covariate. For

number of taxa, we calculated sample-based species accu-

mulation curves and plotted them against increasing volume

of the dead wood substrate.

2.4.3. Data processing and softwarePrior to ANOVAs and regression analyses, logarithmic and

square root transformations were used to normalize the

distributions of the data (if necessary). The analyses were

conducted with PASW Statistics 18.0 for Windows (SPSS

Incorporated) and species accumulation curves were calcu-

lated with EstimateS [40].

3. Results

3.1. Number of occurrences and taxa on FFH and controlclear-cuts

3.1.1. All fungal taxaIn total, we recorded 148 taxa (Supplementary material 1).

107 taxa were recorded on FFH clear-cuts and 128 taxa on

control clear-cuts. The total number of taxa was significantly

lower on FFH than on control clear-cuts at both spatial scales

(Table 2). The species accumulation curves revealed that the

number of taxa was higher on control clear-cuts irrespective

of area (Fig. 2). According to the regression analysis, the

number of taxa was best predicted by the volume of branches

(Table 3).

3.1.2. PolyporesWe recorded 50 species (1347 occurrences) of polypores: 40

species (395 occurrences) on FFH clear-cuts and 41 species (952

occurrences) on control clear-cuts. One near threatened

species [41] was recorded on FFH clear-cuts. In addition, 7

indicator species of old forests [36] were recorded: 6 on FFH

and 4 on control clear-cuts (Supplementary material 1).

The total number of polypore occurrences was lower on

FFH than on control clear-cuts. Polypores G. sepiarium, S.

amorpha and T. abietinum had fewer occurrences on FFH than

on control clear-cuts while the number of F. pinicola occur-

rences did not significantly differ between the treatments. The

number of polypore species was lower on FFH than on control

clear-cuts at plot scale but not at site scale (Table 2). According

to the species accumulation curves, the difference between

FFH and control clear-cuts levelled off with increasing area

(Fig. 2). According to the regression analysis, the volume of

stumps predicted best the number of polypore occurrences

but none of the dead wood variables was significantly related

to the number of polypore species (Table 3).

3.1.3. Saprotrophic agaricswe recorded 86 taxa (21379 occurrences) of saprotrophic

agarics. In total, 58 taxa (8029 occurrences) were recorded

on FFH clear-cuts and 78 taxa (13350 occurrences) on

control clear-cuts. No red-listed or indicator species were

recorded.

The number of saprotrophic agaric occurrences did not

differ between FFH and control clear-cuts. The commonest

species, H. auranthiaca, had more occurrences on FFH than on

control clear-cuts. There was no significant difference in the

number of saprotrophic agaric taxa (Table 2). However,

according to the species accumulation curves, the difference

between FFH and control clear-cuts became more obvious

Table 2e The number of occurrences and species/taxa of fungal groups and occurrences of commonest species (mean ± SD)on forest fuel harvested (FFH) and control clear-cuts and test statistics on the effect of forest fuel harvesting.

FFH control F1,17 p

Total number of taxa/sitea 38.7 � 10.5 47.4 � 16.3 5.029 0.039

Total number of taxa/plotb 16.8 � 6.5 23.0 � 10.0 6.431 0.021

Number of polypore occurrencesa 39.5 � 14.8 95.2 � 44.4 15.23 0.001

Number of polypore species/sitea 13.2 � 3.0 15.3 � 5.2 1.182 0.292

Number of polypore species/plotb 5.7 � 1.9 7.7 � 2.3 6.821 0.018

Number of decomposer agaric occurrencesa 880 � 507 1482 � 1349 1.343 0.263

Number of decomposer agaric species/sitea 21.8 � 7.9 28.0 � 11.9 2.912 0.106

Number of decomposer agaric species/plotb 10.5 � 5.2 14.3 � 7.1 3.138 0.093

Number of pleurotoid agaric occurrencesa 6.4 � 5.4 5.7 � 7.7 0.459 0.507

Number of pleurotoid agaric species/sitea 2.1 � 1.0 2.1 � 2.0 0.179 0.678

Number of pleurotoid agaric species/plotb 0.8 � 0.5 1.0 � 1.1 0.078 0.784

Number of F. pinicola occurrencesa 5.3 � 6.6 10.7 � 10.8 2.688 0.119

Number of Gloeophyllum sepiarium occurrencesa 5.4 � 5.5 21.8 � 17.1 9.887 0.006

Number of S. amorpha occurrencesa 2.3 � 2.8 6.5 � 4.6 7.424 0.014

Number of T. abietinum occurrencesa 3.6 � 3.1 14.3 � 10.9 13.533 0.002

Number of H. auranthiaca occurrencesa 369 � 247 193 � 140 4.527 0.048

a ¼ ANOVA.

b ¼ nested ANOVA.

b i om a s s an d b i o e n e r g y 3 9 ( 2 0 1 2 ) 8 4e9 388

with increasing area, i.e. when several sites were pooled

(Fig. 2). According to the regression analysis, the volume of

branches predicted best the number of saprotrophic agaric

occurrences and taxa (Table 3).

3.1.4. Pleurotoid agaricsWe recorded 12 species (144 occurrences) of pleurotoid

agarics: 9 species (70 occurrences) on FFH clear-cuts and 9

species (74 occurrences) on control clear-cuts. One near

threatened species [42] was recorded on control clear-cuts

(Supplementary material 1).

Fig. 2 e The sample-based species accumulation curves for all

represents increasing area (ha). Black lines represent forest fuel

lines represent means and dotted lines 95% confidence interva

There were no differences in the number of pleurotoid

species and occurrences between FFH and control clear-cuts

(Table 2). Species accumulation curves and regression anal-

ysis were not applied to pleurotoid agarics because of low

number of observations.

3.2. Number of occurrences and taxa on different deadwood substrates

On logs, there were less fungal occurrences on FFH than on

control clear-cuts, but the number of fungal taxa on logs did

fungal taxa, polypores and decomposer agarics. The x-axis

harvested clear-cuts and grey lines control clear-cuts. Solid

ls.

Table 3eTest statistics of the regression analysis exploring the relationship between deadwood variables and the numberfungal occurrences and species. N [ 20. R2 values refer to model including significant (bolded) variables.

R2 Stumps Branches CWD logs FWD logs Old dead wood Inventory date

t p t p t p t p t p t p

Total number of taxa 0.850 �0.083 0.935 3.352 0.004 �0.992 0.336 0.348 0.732 0.449 0.659 7.359 <0.001

Number of polypore occurrences 0.684 5.308 <0.001 0.791 0.441 0.290 0.775 0.183 0.857 0.955 0.354 2.184 0.043

Number of polypore species 0.436 1.341 0.198 0.856 0.404 0.341 0.737 0.850 0.407 0.764 0.455 3.728 0.002

Number of saprotrophic agaric

occurrences

0.703 0.219 0.829 2.796 0.012 �0.746 0.466 �0.449 0.660 �0.229 0.881 4.493 <0.001

Number of saprotrophic agaric taxa 0.719 0.190 0.852 2.464 0.025 �0.996 0.334 �0.040 0.969 0.518 0.611 4.997 <0.001

b i om a s s a n d b i o e n e r g y 3 9 ( 2 0 1 2 ) 8 4e9 3 89

not differ between FFH and control clear-cuts (Table 4). The

difference in the number of occurrences was significant also

after controlling for log volume (Fig. 3). The species accumu-

lation curves against increasing log volume did not differ

between the treatments (Fig. 4).

On stumps, there were less fungal occurrences and taxa

and on FFH than on control clear-cuts (Table 4). The number of

occurrences on stumps did not differ between the treatments

after controlling for stump volume (Fig. 3), and the species

accumulation curves revealed that there were slightly more

species per given stump volume on FFH clear-cuts (Fig. 4).

On branches, there were no differences between FFH and

control clear-cuts in the number of fungal taxa and occur-

rences (Table 4). The number of occurrences did not differ

between the treatments after controlling for branch volume

(Fig. 3), nor did species accumulation curves against

increasing volume of branches (Fig. 4).

4. Discussion

4.1. Main findings

Forest fuel harvesting reduced strongly the number of polypore

occurrences and also decreased the total number of fungal taxa

and the number of polypore species. However, the effect on the

number of polypore species was significant only at plot scale

anddecreasedwith increasingarea. Incontrast, theeffect on the

number of saprotrophic agaric taxa was not significant at small

scales but became evident with increasing area. Most of the

common polypore species had fewer occurrences on FFH clear-

cuts but the commonest agaric had more occurrences there.

Concerning thedifferent types ofdeadwood, thenegative effect

of FFH wasmost obvious among stumps. The effect of FFH was

mainly due to the reduction in resource availability.

Table 4 e The number of fungal occurrences and taxa (mean ±harvested (FFH) and control clear-cuts and test statistics on th

FFH

Number of taxa on logs 12.2 � 4.3

Number of occurrences on logs 25.1 � 12.0

Number of taxa on stumps 4.5 � 2.6

Number of occurrences on stumps 9.0 � 6.6

Number of taxa on branches 5.4 � 2.4

Number of occurrences on branches 8.2 � 4.4

4.2. Effect of forest fuel harvesting on polypores

The total number of polypore species recorded (50) was

notably high. Compared to other managed forest habitats, we

found more species on clear-cuts (on average 14 species per

0.16 ha area) than has been reported e.g. on woodland key

habitats (surroundings of small brooks; on average 10 species

per 0.2 ha area) [43]. Our results are consistent with earlier

studies which have shown the first stage of succession to host

highest polypore diversity in natural as well as managed

forests [28]. On clear-cuts, the volume and diversity of dead

wood is low compared to the corresponding successional

stage in natural forests, but the wealth of fresh logging resi-

dues and stumps still provide habitat for pioneer species and

some residual logs may host species preferring later decay

stages [28,44].

The number of polypore occurrences was substantially

lower on FFH clear-cuts. This is obviously due to FFH

removing resources such as stumps and small-diameter logs

that are efficiently utilized by several species preferring

fresh dead wood. At small scale, there was also a difference

in the number of species between FFH and control clear-

cuts. However, this difference levelled off with increasing

area. Such pattern could arise from FFH decreasing the

amount of abundant resources while the amount of rare

resources such as large logs and old dead wood remains

more or less unaffected. Therefore, FFH primarily affects the

density of common species that may thus becomemissed on

a small area but can still be found if a large area enough is

covered.

A few red-listed or indicator polypores were recorded on

the clear-cuts. However, they were mainly found on

substrates not affected by FFH and thus FFH is unlikely to

threaten these species. However, the decline of the common

species is by no means unimportant and gives also cause to

SD) on the commonest dead wood substrates on forest fuele effect of forest fuel harvesting.

control F1,17 p

15.5 � 7.5 1.702 0.209

51.9 � 31.8 7.020 0.017

9.9 � 4.7 10.456 0.005

41.8 � 2.8 16.933 0.001

8.0 � 6.0 1.667 0.214

25.2 � 36.9 1.928 0.183

b i om a s s an d b i o e n e r g y 3 9 ( 2 0 1 2 ) 8 4e9 390

another concern. As major decayers of wood, polypores

provide habitats and modulate the resources suitable for

a wealth of other organisms dependent on dead wood [2,13].

Polypores also have an essential role in nutrient recycling, soil

formation and carbon budget of forest ecosystem [13].

Therefore, the decrease of polypores may substantially affect

other dead wood dependent organisms and even the function

of forest ecosystem.

4.3. Effect of forest fuel harvesting on saprotrophicagarics

There was no difference in the number of saprotrophic agaric

occurrences between FFH and control clear-cuts. However,

this pattern was due to the commonest species, H. aurantiaca,

clearly benefiting from FFH. Indeed, H. aurantiaca accounted

for 46% of saprotrophic agaric occurrences on FFH clear-cuts

but only 14% on control clear-cuts. The species is very

common in Finland and it evidently benefits from distur-

bances, warmth and sun-exposure. It is difficult to judge the

general ecological importance of the increased dominance of

this species, but it may be considered as a signal of an

increasingly disturbed ecosystem.

The number of saprotrophic agaric species did not signifi-

cantly differ between FFH and control clear-cuts at plot and

site scales, but contrary to polypores, the difference between

the treatments became obvious with increasing area.

Fig. 3 e The number of fungal occurrences on logs, stumps and

substrate on forest fuel harvested (black circles) and control cle

treatment effect after controlling for volume.

However, the lack of statistical significance at smaller scales

can be attributed to the substantial within-treatment varia-

tion which may actually be due to variation in fruit body

production (see below). FFH can potentially have stronger

effect on agarics than on polypores, because a substantial

proportion of agaric species depend on small-diameter dead

wood. For example, the agaric species growing from the forest

floor frequently decompose the smallest dead wood pieces

and needle litter [45], i.e. resources that decline on clear-cuts

when branches are removed. These species are also likely to

be affected by the increased intensity of soil disturbance

caused by FFH [46].

4.4. The importance of different dead wood substrates

In natural forests, logs are the most important substrate for

fungi [47]. Also in this study, logs hosted the highest number

of fungal occurrences and taxa (Table 4). Logs also formed the

majority of dead wood especially on FFH clear-cuts [11]. The

volume of logs did not significantly differ between FFH and

control clear-cuts [11], but the number of fungal occurrences

on logs was higher on control clear-cuts. This difference

remained significant also after controlling for log volume. This

may be due to FFH altering the composition of logs, i.e.

decreasing the number of fresh small logs that hold relatively

high number of fungal occurrences. However, the number of

fungal taxa on logs did not differ between FFH and control

branches in relation to the volume (m3) of the particular

ar-cuts (open circles). The test statistics represent the

Fig. 4 e The sample-based species accumulation curves for

fungal taxa growing on logs, stumps and branches. The x-

axis represents increasing volume (m3) of the particular

substrate. Black lines represent forest fuel harvested clear-

cuts and grey lines control clear-cuts. Solid lines represent

means and dotted lines 95% confidence intervals.

b i om a s s a n d b i o e n e r g y 3 9 ( 2 0 1 2 ) 8 4e9 3 91

clear-cuts, and the species accumulation curves against

increasing log volume were identical. Therefore, the logs

removed by FFH apparently have a low contribution to the

number of species.

Stumps are likely to be of importance in maintaining the

species richness of fungi in managed forests [28,30]. For

example, it has been reported that in 50 years old spruce

forests there were notably more species on stumps than on

e.g. branches or treetops, and stumps also hosted the highest

number of unique species [30]. In this study, there were 81%

less stumps on FFH clear-cuts than on control clear-cuts [11].

Consequently, FFH had a strong negative effect on the number

of fungal occurrences and taxa on stumps. The difference in

the number of occurrences was totally explained by the

difference in stump volume, because the number of occur-

rences did not differ between the treatments after controlling

for volume. The species accumulation curves revealed that

there appeared to be more fungal taxa per given stump

volume on FFH clear-cuts. This may be due to FFH not

affecting stumps originated from the earlier logging events.

These stumps are a rare resource but their proportion of the

stump volume increases due to FFH. Thus, per given stump

volume there may be more rare species occupying rare

substrates on FFH clear-cuts.

Although the average volume of branches was 42% lower

on FFH clear-cuts than on control clear-cuts [11], FFH did not

significantly affect the fungi growing on branches. The

number of fungal occurrences and taxa on branches was

generally low, but it must be noted that the volume of

branches was actually the best predictor of total number of

fungal taxa and number of saprotrophic agaric occurrences

and taxa on a study site. This suggests that branches may

have some additional effects on fungi (they may e.g. be

important for species growing from the forest floor) and that

harvesting of branches is likely to have harmful effects on

fungal diversity. The importance of branches may be

pronounced during dry years when branches have been re-

ported to be particularly important for agarics [32]. The

microclimate remains more stable in areas where branches

are left, while the removal of branches and foliage increases

the wind speed and temperature fluctuations both below and

above ground [48].

4.5. Methodological notes

Field inventories of fungi are often based on observations of

fruit bodies. However, the sporadic fruit body production

hampers the detectability of fungi, and the whole species pool

can never be covered in a single survey [49]. In addition, the

results of the survey are sensitive to the timing of the inven-

tory and to the local weather and light conditions that strongly

affect fruit body production [50]. This is particularly true for

agarics that produce relatively short-lived fruit bodies. In

contrast, a substantial proportion of polypores produce

perennial fruit bodies that are detectable throughout the year,

and also the fruit bodies of the annual polypores may remain

detectable and identifiable for a longer time than those of

agarics [49].

In our study, it was evident that inventory date affected the

number of occurrences and species recorded and that the

effect was strongest among agarics. Although we were able to

control for the effect of inventory date, it is likely that there

was still much uncontrolled variation in the fruit body

production of agarics due to the local conditions. Such varia-

tion can easily hinder observing consistent treatment effects.

We conclude that using repeated surveys [49] would greatly

improve the reliability of fungal studies, and that controlling

for the timing of the survey should be a minimum

requirement.

4.6. Long-term effects of forest fuel harvesting

We agree with a recent modelling work [51] that resource

depletion caused by FFH is not likely to lead to immediate local

extinctions. However, the first effects of habitat degradation

on the number of species can already be seen especially at

small scale. In the long run, if the regional populations of

species preferring early successional stages continue to

decline, even some of the today’s common species may

become threatened.

It is likely that the effects of stump removal will become

more obvious with time. Stumps are a longer-lasting resource

for wood-decaying species than logging residues, because

largepiecesofwooddecay slower thansmaller ones [52]. Based

on the model of decomposition rate [53] the time required to

the loss of 95% of the wood is 64 years. Thus, stumps may

b i om a s s an d b i o e n e r g y 3 9 ( 2 0 1 2 ) 8 4e9 392

provide refuges for forest species after logging residues and

logs from the pre-cutting period have decayed and before new

dead wood has started to accumulate. Therefore, to maintain

the dead wood continuum in managed forests it would be

essential to leave more stumps on FFH clear-cuts.

5. Conclusions

Clear-cuts provide habitat and resources for species favouring

early successional stages and our study confirms that they

host relatively rich fungal assemblages. Previous work has

shown that forest fuel harvesting causes a substantial change

in resource availability on clear-cuts and can thus affect the

fungal diversity of managed forests. In this study, we found

that forest fuel harvesting leads to the decline of decomposer

fungi, this beingparticularly obvious among commonpolypore

species. On the other hand, forest fuel harvesting may benefit

somespecies that favour intensive disturbances. There is a risk

that populations of certain species will strongly decline

throughout landscapes or regions if forest fuel harvesting

becomes established as a common practice in boreal forests.

Acknowledgements

We thank the editors and an anonymous reviewer for valuable

comments.We are grateful to Timo Kosonen, ElinaManninen,

Katriina Peltonen, Emmi Lehkonen, Noora Vartija, Mikko

Sorjanen and Elisa Markkanen for help in the field work, and

Heikki Kotiranta, Tuomo Niemela and Jukka Vauras for iden-

tification of some specimens. Co-operation with Jari Haimi,

UPM, Metsahallitus and city of Jyvaskyla made it possible to

establish the experiment. This study was supported finan-

cially by Ministry of Agriculture and Forestry, Metsamiesten

Saatio Foundation, Societas Biologica Fennica Vanamo and

Centre of Excellence in Evolutionary Research.

Appendix. Supplementary material

Supplementary material associated with this article can be

found, in the online version, at doi:10.1016/j.biombioe.2011.11.

016.

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